Morphological Variation of the Newly Confirmed Population of the Javelin Sand Boa, Eryx Jaculus (Linnaeus, 1758) (Serpentes, Erycidae) in Sicily, Italy

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Acta Herpetologica 14(2): 135-139, 2019 DOI: 10.13128/a_h-7752

Morphological variation of the newly confirmed population of the Javelin sand boa, Eryx jaculus (Linnaeus, 1758) (Serpentes, Erycidae) in Sicily, Italy

Francesco P. Faraone1,*, Salvatore Russotto2, Salvatore A. Barra3, Roberto Chiara3, Gabriele Giacalone4, Mario Lo Valvo3 1 Viale Regione Siciliana S.E., 532, 90129 Palermo, Italy 2 Contrada Grassura Mollaka Faia, s.n., 92027 Licata (AG), Italy 3 Dipartimento Scienze e Tecnologie Biologiche, Chimiche e Farmaceutiche, University of Palermo, Via Archirafi, 18, 90123 Palermo, Italy 4 Cooperativa Silene, Via D’Ondes Reggio, 8/a, 90127 Palermo, Italy *Corresponding author. Email: [email protected]

Submitted on: 2019, 13th May; revised on: 2019, 20th June; accepted on: 2019, 29th June Editor: Dario Ottonello

Abstract. The presence of the Javelin sand boa in Sicily has recently been confirmed. Here the morphological characters and sexual dimorphism of the Sicilian population of Eryx jaculus are presented. Seven meristic and six metric characters in 96 specimens from Sicily were examined. The results show that tail length, snout-vent length, the distance between nostrils and the number of ventral and subcaudal scales are different between sexes. The characters found in the Sicilian population of the Javelin sand boa resemble those of the African population (ssp. jaculus) rather than the Eurasian population (ssp. turcicus), but biomolecular studies are necessary to understand its taxonomic iden- tity.

Keywords. Eryx jaculus, Serpentes, morphological variation, folidosis.

The Javelin sand boa Eryx jaculus (Linnaeus, 1758), Recently, the presence of E. jaculus has been con- a member of the family Erycidae, is found in the south- firmed in a small area of southern Sicily, in Italy (Insacco ern Balkans, Middle East and North Africa (Sindaco et et al., 2015). Knowledge of the Javelin sand boa in Sicily al., 2013). Two morphologically defined subspecies are is currently limited to scant preliminary information on usually recognized for this species. The nominate sub- the population’s distribution, morphology, habitat and species is present in North Africa and the ssp. turcicus diet (Insacco et al., 2015; Faraone et al., 2017a, b). (Olivier, 1801) is found in the Balkans and the Mid- In this paper the first comprehensive report of the dle East (Tokar and Obst, 1993; Sindaco et al., 2013; morphological characters and sexual dimorphism in the Geniez, 2015). According to Tokar and Obst (1993), Sicilian population of E. jaculus is presented. the Transcaucasian ssp. familiaris Eichwald, 1831 Sampling was carried out within the currently known could be synonymous with E. j. turcicus. Morphologi- geographic range of the Javelin sand boa in South Central cal variations of E. jaculus have been reported both at Sicily, within an area between Palma di Montechiaro (prov- a global (Tokar, 1991) and a local scale (Cattaneo, 1984, ince of Agrigento) and Butera (province of Caltanissetta) 2005, 2010; Rhadi et al., 2015; Zarrintab et al., 2017; (see Insacco et al., 2015; Faraone et al., 2017b). A total of Eskandarzadeh et al., 2018). 55 adult (30 males; 25 females) and 41 juvenile (21 males;

ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah 136 Francesco P. Faraone et alii

b 17 females; 3 undetermined) specimens were examined Z =Yi (SVL/ SVLi ) between August 2014 and September 2018. Among them, 47 specimens were collected during active searches at night, following Lleonart et al. (2000), where Z is the trans- 12 specimens were rescued from abandoned cisterns and formed value of the variable Y, which is the variable the tunnel greenhouse in which they were trapped, four affected by size, represented as the snout-vent length were found dead inside cisterns, one had been killed by (SVL), and b is the slope of the linear regression between domestic cats and 32 specimens were roadkilled. logY and logSVL. The data were checked for parametric Sex was determined by examining external sexual assumptions using Levene’s test and the Shapiro-Wilk features (spurs, tail shape) and, mainly in young snakes, test. For each variable, parametric (independent t-test) also by cloacal popping. The reliability of external fea- or non-parametric (Mann-Whitney U test) analysis was tures for sexual determination was also confirmed by conducted, with a level of significance at 0.05. Differ- cloacal probing in dead specimens. In absence of detailed ences between the sexes were checked by using the Prin- references, E. jaculus with a snout-vent length < 270 mm cipal Component Analysis (PCA), applied to the cor- (see Itescu et al., 2018; Eskandarzadeh et al., 2018) were relation matrix. Body weight (W) was not included in considered as juveniles. PCA, because its value can vary greatly depending on the Seven meristic characters were considered: the num- condition of each specimen (pregnancy, decay, freshly ber of scales between the eyes (BE), around the eye (RE), ingested prey, etc.). SVL and the characters with a P value posterior to the internasal (PIN), between the eye and the greater than 0.05 were also excluded. nasal (BEN), the rows of scales between the eye and the Color morph was classified according to the three supralabial area (BES), the ventrals (VS) and the subcaudals types reported by Tokar (1991) and Tokar and Obst (ScdS). Six metric characters were also recorded: snout-vent (1993). The ‘discrete’ morph is characterized by a reduced length (SVL), tail length (TL), the distance between the dorsal pattern, with narrow transverse dorsal bars and eyes (DBE), the distance between the posterior edge of the small scattered spots on the sides. In the ‘standard’ eye and the tip of the snout (DES), the distance between morph, the dorsal pattern is more extensive than in the the nostrils (DBN) as well as body weight (W). For bilat- ‘discrete’ morph and the dorsal blotches are spaced by eral characters, only the right side was recorded. Biometric light areas of similar thickness and are not in contact characters were measured using a digital caliper accurate to with each other. The ‘negative’ morph is characterized by 0.01 mm, except for SVL, which was measured with a mm a greater development of the dark pattern, while the light ruler, and body weight (W), which was measured only on parts are reduced to narrow suboval blotches on the back. live individuals using a digital scale with 1 g precision. The descriptive statistic and a comparison between In order to remove the information related to size, sexes were made for adults (Table 1). Significant inter- each metric variable was transformed using the formula: sexual differences in five characters were found: the num-

Table 1. Descriptive statistics and univariate comparisons between sexes of the Sicilian population of Eryx jaculus. The first five characters are in millimetres, the sixth in grams and the others are meristic. Significant differences (P<0.05) are shown in bold. *= transformed values.

Males Females T U P Mean ± SD Range n Mean ± SD Range n SVL 342.1 ± 42.4 270.0 - 420.0 26 400.5 ± 86.1 270.0 - 580.0 23 3.2 - 0.004 *TL 40.7 ± 6.0 26.9 - 53.9 26 31.4 ± 6.2 20.7 - 45.9 23 7.9 - 0.000 *DES 7.1 ± 0.7 5.8 - 8.7 26 7.6 ± 1.2 5.9 - 10.5 21 1.8 - 0.086 *DBN 4.0 ± 0.4 3.3 - 4.7 26 4.2 ± 0.6 3.3 - 5.6 21 2.4 - 0.019 *DBE 7.0 ± 0.7 6.1 - 8.3 26 7.5 ± 1.1 5.5 - 10.0 21 - 165.0 0.194 W 36.9 ± 19.5 18 - 95 14 64.2 ± 49.6 15 – 204 16 - 76.0 0.135 VS 175.9 ± 2.8 170 - 182 26 181.9 ± 3.9 176 - 190 21 6.1 - 0.000 ScdS 25.2 ± 1.9 22 - 29 29 19.7 ± 1.4 17 - 22 23 11.8 - 0.000 PIN 2.6 ± 0.5 2 - 3 30 2.6 ± 0.5 2 - 3 24 - 357.0 0.958 BE 6.8 ± 0.6 6 - 8 30 6.8 ± 0.4 6 - 7 24 - 358.0 0.972 RE 9.4 ± 0.8 8 - 11 29 9.0 ± 0.7 8 - 10 22 - 238.5 0.126 BEN 3.0 ± 0 3 - 3 30 3.0 ± 0 3 - 3 24 - - - BES 1.0 ± 0.2 1 - 2 30 1.0 ± 0 1 - 1 24 - 348.0 0.835 Morphological variation of Eryx jaculus in Sicily 137

Fig. 1. Scatterplot of scores with the equiprobability ellipses at 95% projected on the first two principal components between sexes of Fig. 2. Examples of color and pattern variation in the Sicilian popu- the Sicilian population of Eryx jaculus. lation of Eryx jaculus. (A) Adult, male (B) Adult, female (C) Juve- nile, male (D) Ventral variation in three adult females. ber of ventral scales and snout-vent length have higher the ‘negative’ phenotype, but some small parts of their values in females and the number of subcaudal scales, back looked like the ‘standard’ morph, similar to what the distance between the nostrils and the tail length have was observed in some E. jaculus by Tokar and Obst higher values in males. The result of the Principal Com- (1993) and Werner (2016). Young individuals were gener- ponents Analysis (PCA) shows that 85.1% of the vari- ally lighter than adults, with a lower contrast in the dark ance is explained by the first two components (PC1 = pattern. No difference in dorsal color pattern was noticed 58.1%, PC2 = 27.0%). The scatterplot of scores with the between sexes. The dorsal base color is orange, sand or equiprobability ellipses at 95% (Lagonegro and Feoli, yellowish. The ventral, paraventral and some adjacent 1985) projected on the first two principal components scales were usually pale yellowish orange (in only one (Fig. 1) shows a clear separation between sexes on PC1, large female it was a whitish-cream color). Ventral parts with males distributed within the negative values of the were adorned with small blackish spots. The orange color axis and the females within the positive values. of the belly in a few cases extended to the subcaudal The correlation coefficients of the variables (Table 2) scales, which usually appeared whitish with a few scat- show that PC1 has a strong positive correlation with ven- tered orange scales. tral scales (VS) and a negative correlation with subcaudal The results show clear intersexual differences in the scales (ScdS) and tail length (TL). Sicilian population of E. jaculus. The females usually The examined specimens showed different color pat- reach a greater size in terms of snout-vent length and terns (Fig. 2). In most of the snakes, the ‘standard’ morph have a greater number of ventral scales than males, and was identified, however in some individuals the dorsal males have a greater number of subcaudal scales, a longer dark blotches were so extended that they appeared simi- tail and a greater distance between the nostrils. Signifi- lar to the ‘negative’ morph, yet these spots were not con- cant intersexual differences in ventral scales have already nected on the sides, so they were assigned to the ‘stand- been observed in this species (Tokar, 1991) but are not ard’ type. Seven snakes could generally be attributed to found in some Asian populations (Rhadi et al., 2015; Eskandarzadeh et al., 2018) nor in some other Eryx species (Al-Sadoon and Al-Otaibi, 2014; Eskandarzadeh et Table 2. Correlation coefficients of the variables for the first two al., 2013). factors used in the Principal Component Analysis (PCA). The pattern of sexual dimorphism observed in the Variables PC 1 PC 2 Sicilian population is also reported in other species of snakes (Marques et al., 2006, Pizzatto et al., 2007, Zanella TL -0,81 0,52 and Cechin, 2010, Siqueira et al., 2013, Manjarrez et al., DBN -0,40 -0,88 2014). Larger females can provide more space for incu- VS 0,81 0,16 bating eggs and embryos and more body reserves to ScdS -0,92 0,07 138 Francesco P. Faraone et alii invest in reproduction (Bonnett et al., 1998) and gener- tively (see also Tokar, 1991). The morphological affinities ally, have a larger clutch size (Shine, 1993) and lower between the Sicilian and African populations reported mortality in their offspring (Kissner and Weatherhead, here has only a preliminary value and, obviously, a bio- 2005). Moreover, in various snake species the number of molecular approach is necessary in order to properly ventral scales corresponds to the number of dorsal ver- assess the phylogeographic and taxonomic structure of tebrae, which are generally more numerous in the larger the Javelin sand boa. sex (Shine, 2000). On the other hand, smaller males have greater agility during the search for females and a lower metabolic cost (Rivas and Burghardt, 2001). A larger tail ACKNOWLEDGEMENTS and a greater number of subcaudal scales in males are linked to the positioning of the hemipenes within the tail We are grateful to Agostino Cantavenera, Matteo and produce better performance in the courtship phase Di Nicola, Angelica Rallo, Alex Venutelli for their help (King, 1989; Luiselli, 1996; Shine et al., 1999). The males in fieldwork. We also thank Edoardo Razzetti for kindly of Sicilian E. jaculus also have a relatively larger interna- providing us some interesting bibliographic references sal distance (DBN) than the females. Sexual dimorphism and Viviana Tinnirello for language revision. The tem- in head shape is a phenomenon known in various snake porary capture and handling have been carried out with species and is often linked to a different trophic niche the permits established by law (MATT prot. N.2766 / between males and females (Camilleri and Shine, 1990; T-A31, 12/01/2018 and Regione Siciliana Prot. N, 1637, Vincent et al., 2004). 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